L
THE
CONDOR
A JOURNAL OF AVIAN BIOLOGY
Volume 91
Number 3
August 1989
The Condor91:505-514
0 TheCooperOrnithological
Society1989
THERMOREGULATION
IN TURKEY VULTU
VASCULAR ANATOMY,
ARTERIOVENOUS
HEAT EXCHANGE,
AND BEHAVIOR’
#RARY.
.
A, lr, 2 2 1989
ZEEV ARAD
Department of Biology, Technion,Haifa 32000, Israt;
~i-~~~~~~~~~
OF
W-IO
UFFE MIDTG~D
Institute of Cell Biology and Anatomy, Universityof Copenhagen,DK-2100 Copenhagen0, Denmark
MARVIN
H.
BERNSTEIN
Department of Biology,New Mexico State University,Las Cruces,NM 88003
Abstract. The vasculatureof skin and of peripheralheatexchangers
in Turkey Vultures
(Cathartesaura, mass 1.4 kg)wasstudiedin relationto peripheraltemperatures
andbehavior
at ambienttemperatures
(TJ from 10°Cthrough50°C.The head’sunfeathered
skincontains
thin-walled,anastomosing
veins near the epidermis.Metatarsalskin hasa similar venous
plexus, but cutaneousvasculaturefrom the wing’s underside does not. Skin temperature
(TJ at the crown was close to T, but T, at the nape was close to body temperature (Tb). At
both skin sitesT, changedwith T,. Investigation of deepervasculatureshowedthat the head
has bilateral ophthalmic retia that probably cool the brain and eyes, as in other birds. In
the wing, the basilica vein branchesto form a venae comitantes, a mesh of anastomosing
veins that separatelysurroundsthe radial and ulnar arteries. A bypassvein is also present.
The temperatureprofilesalong the IO-cm length of this humeral plexusbecame steeperwith
decreasingT,. At its distal end, temperaturefell to 22°C at 10°CT,, with the steepestobserved
gradient being 3.0”Ucm. In each leg, the tibia1 and fibular arteries closely contact two to
four venae comitantes to form a simple rete, as in other species.This helps conservebody
heat in cold but, as in the wing, is probably bypassedduring heat stress.Behavior ranged
from neck and wing retractionwith a pale head and feet at low T,, to neckand wing extension
with a deep red head and feet at high T,. Panting, gular flutter, and urohidrosisaccompanied
these responsesat the highest T,s.
Key words: Cathartesaura;Falcomformes;heat loss;heat transfer;peripheral vascular
anatomy; skin vasculature;temperatureregulation;Turkey Vulture.
INTRODUCTION
Turkey Vultures (Cuthartes aura) range from
southern Canada throughout the United States
to Central America. The populations at the
northernmost edge of their range depart in autumn, but may still be exposedto winter storms
when they return to their breeding areas (Hatch
1970), whereaspopulations in tropical and desert
habitats experience humid and dry heat. Encountering a wide variety of climates, Turkey
LReceived 12 September 1988. Final acceptance30
March 1989.
Vultures have apparently evolved diverse mechanisms to cope with thermal extremes.
Mechanisms that help Turkey Vultures tolerate cold include reducing body temperature to
save energy and seeking shelter in caves (Heath
1962, Hatch 1970). High-temperature tolerance
relies on both physiological and behavioral adaptationsto dissipateheat. Turkey Vultures, when
heat stressedin a metabolic chamber, regulated
their body temperaturesonly by evaporation and
reduced insulation, the chamber being too small
to allow postural adjustments that increase heat
loss(Arad and Bernstein 1988). In the field, however, Turkey Vultures exposed to high ambient
506
Z. ARAD, U. MIDTGMD
HEAT CONSERVING
AND
M. H. BERNSTEIN
STRUCTURES
(AV HEAT EXCHANGERS)
POTENTIAL
HEAT LOSS
AREAS
NAKED HEAD
BEHAVIOR
ENHANCING
HEAT LOSS
STRETCHING
OF NECK
AND NECK
OPHTHALMIC
RETE
HUMERAL COMPLEX
TIBIOTARSAL
WING UNDERSIDE
SPREAD-WING
POSTURE
RETE
NAKED FEET
UROHIDROSIS
FIGURE 1. Summarvof differentareasand behaviorsthat are important in thermoregulation
by Turkey
Vultures.
temperature extend the unfeathered head and
neck, expose the poorly feathered undersides of
the wings, and urinate on the legs.
Arteriovenous, countercurrent heat exchangers are present in the heads, wings, and legs of
many avian species(Midtgard 1988) and would
be expectedto help reduce heat loss during cold
exposure. Reduced peripheral blood flow, especially in the naked skin of the head, neck, legs,
and feet of Turkey Vultures, would also be expectedto reduce heat loss, whereasincreasedcutaneous blood flow would accelerate heat dissipation during heat stress.In evaluating areas of
unfeathered skin as potential heat-losspathways,
it is important to know their degreeof vascularization. There are, however, no studies dealing
with this topic, nor with the gross anatomy of
arteriovenous (AV) heat exchangers,in Turkey
Vultures.
The objectives of this study were therefore to
describe the anatomy of the heat-exchange systems and skin vasculature in Turkey Vultures
and thereby to establisha structural basisfor part
of their thermoregulatory repertoire (Fig. l), then
to correlate the morphology with preliminary
temperature and behavioral observationsthought
to be part of that repertoire.
MATERIALS
AND METHODS
ANATOMY
Five adult, captive Turkey Vultures (mean body
mass 1.4 kg) were kept in an outdoor aviary and
offered commercial bird-of-prey diet and water
ad libitum, as previously described (Arad and
Bernstein 1988). One bird that died during a previous study had been frozen. After thawing, its
circulatory system was injected with latex (Microfil, Canton Biomedical Products), and then it
was fixed by immersion in a mixture of alcohol,
formaldehyde, and acetic acid (AFA). A second
bird was anesthetized with inhaled halothane,
cannulated in the brachial, cephalic, and sciatic
arteries, and then given an overdose of anesthetic. The cannulae were perfused with warm,
heparinized, isotonic saline, then with AFA. After fixation, samples of various skin areas and
vascular complexes were removed and embedded in paraplast. The sections(lo-12 wrn thick)
were stained with hematoxylin and eosin. The
nomenclature applied to the observed vasculature follows the Nomina Anatomica Avium (Baume1 et al. 1979).
TEMPERATURE MEASUREMENTS
To demonstrate the possible physiological significance of the morphological findings, we undertook preliminary measurements of temperature in presumed heat-exchange areas. To
evaluate countercurrentheat exchangein the wing
we measuredtemperature gradientsalong the humeral vascular complex in two vultures. On the
day of an experiment, a bird was lightly restrained and locally anesthetizedin the underside
of one wing by subcutaneous injection of lidoCaine (2%). A 15-cm-long incision was made in
the humeral region and five insulated, 36-gauge,
copper-constantan thermocouples were sutured
to muscle with their junctions at fixed intervals
TURKEY VULTURE VASCULATURE
along the humeral plexus. The skin was then sutured. To enable observations of skin temperatures in unfeatheredregionsofthe head and neck,
thermocouples were also inserted subcutaneously at the crown and the nape. For measurement of core body temperature (T,,), a thermocouple was placed in the cloaca to a depth of
about 5 cm and tied to the rectrices.
The bird, with its eyes covered, was placed
upright on a canvas sling mounted in a darkened,
controlled-temperature chamber (* 0.K). The
legsprotruded through holes in the sling and the
wings were above the edges of the sling, so all
four limbs remained unrestrained. The thermocouples extended through a small hole in the
chamber wall and were connected to a digitizing
data logger(Campbell Scientific, 2 1X) which calculated the means of 60 measurementsfrom each
thermocouple every minute. The data-logger
output was directed to a microcomputer that displayed and recorded the temperatures to the
nearest0.0 1°C.Another thermocouplewas placed
near the bird in the chamber to measure ambient
temperature (TJ, which was displayed on a digital thermometer (Bailey, Thermalert TH8). Prior
to experiments, all thermocouples were calibrated against a mercury-in-glass thermometer
having an accuracy(f 0. 1“C) traceableto the U.S.
National Bureau of Standards.
The T, washrst setat 30°C (29.8-30.2%), which
is within the zone of thermal neutrality for this
species.For one vulture, T, was changedto 10°C
(9.8-10.2%) then to 40°C (39.8-40.2”Q whereas
for the other vulture T, was changedto 40°C then
to 10°C. Each T, was maintained until a thermal
steady statewas observed(1.0-l 5 hr); data were
then recorded for at least 16 min.
BEHAVIORAL OBSERVATIONS
To gain preliminary information on behavior in
relation to putative heat-exchange surfaces, an
unrestrained Turkey Vulture was enclosedin the
controlled-temperature cabinet with ample space
to move about and change its posture. It was
illuminated by the light from an incandescent
lamp and observed from a darkened room
through a small glass window in the chamber
door. The bird was held at a T, of 10, 20, 30,
40, 45, 50, or 53°C for 1.0-1.5 hr and posture,
behavior, and color of the naked skin were observed and noted. Core T, was measured in the
cloaca at the end of the exposure to 53°C and
after recovery at T, of 35°C.
AND THERMOREGULATION
507
RESULTS
ARTERIOVENOUS
HEAT EXCHANGERS
Head.The pattern ofthe major arteriesand veins
in the head (Fig. 2) conforms to that observed
in other bird species.There are well-developed,
bilateral ophthalmic retia with a high degree of
AV contact (Fig. 3a). The numbers of arteries
and veins in a rete are about 100 and 50, respectively. The main efferent arteries from the
rete are the ophthalmotemporal and supraorbital
arteries, which supply the eye and periorbital
structures, but which also anastomose with the
ethmoidal artery leading to the brain. The main
venous tributaries to the rete are the ophthalmotemporal, supraorbital, and palpebral veins,
which may receive blood from the eye, nasal
cavity, and the skin surrounding the eye.
Wing.The wing is supplied and drained by the
brachial artery and the basilica vein, respectively. The brachial artery divides into the radial and
ulnar arteries. These parallel each other nearly
throughout the length of the wing, as shown in
Figure 4, and are each enmeshed in the humeral
region by a surprisingly well-developed system
of venae comitantes. In crosssection this system
appears to consist of four to nine veins in close
contact with, and completely enveloping, each
artery (Fig. 3b). In the distal part of the wing,
the ulnar and radial arteries are each paralleled
by only two veins (Fig. 4). The large, separate
basilica vein, which constitutes the major drainage of the wing, courses independently in the
distal part of the wing, anastomoses with the
venae comitantes system of the radial and ulnar
arteries near the elbow, and then bypassesthe
heat-exchangesystem in the humeral region.
Leg.As shown in Figure 5, most of the arteries
in the lower leg are accompanied by veins, but
the degreeof AV contact is most extensive in the
distal part of the tibia1 region. Sections of the
cranial tibia1 vascular complex at this level show
a large artery (the cranial tibia1 artery) and three
collateral arteries (branchesof the fibular artery,
Fig. 3c) which are all in contact with two to four
venae comitantes. Together these arteries and
veins form a rete mirabile, although it is extremely simple.
SKIN VASCULARIZATION
Head and neck.Compared with the feathered
part of the neck (Fig. 3d), the naked skin of the
head is extremely well vascularized (Fig. 3e). In
508
Z. ARAD, U. MIDTGARD
AND
M. H. BERNSTEIN
FIGURE 2. Outline of the major cephalic arteries in Turkey Vultures. For clarity, only some of the veins
(black) have been shown. Arteries supplying the skin are marked with asterisks. 1, A. carotis interna; 2, A.
comes N. vagi; 3, A. esophagealisdescendens;4, A. trachealis descendens;5, A. occipitalis; 6, A. palatina; 7,
A. lingualis; 8, A. ophthalmica extema; 9, R. occipitalis; 10, Rete ophthalmicurn; 11, A. supraorbitalis; 12, A.
& V. ophthalmotemporalis; 13, A. & V. ethmoidalis; 14, A. facialis. Scalebar equals 1 cm.
the superficial part of the cutaneous tissue, just
below the epidermis, are one or two layers of
thin-walled, anastomosing veins. Typical AV
anastomoses (AVAs) as seen,for example, in the
collar plexus of the pigeon (Baumel et al. 1983)
and in the nasal mucosa of the duck (Midtgard
1984) were not observed to be associatedwith
this cutaneous plexus. The venous plexus in the
skin of the vulture’s head appears instead to be
supplied directly from slender arterioles originating from larger arteries located beneath a
prominent subcutaneouslayer of smooth muscle
cells. The venous plexus in the skin of the crown
and nape drains into the facial vein which appears to connect to the nasal vein, leading into
the superficial occipital veins and into small
branches leading directly to the jugulars.
Wing. Histological sectionswere made of the
skin from several areas of the underside of the
wing, but AVAs were not found, nor did the skin
appear to have an unusual degreeof vascularity
that could be claimed to have special thermoregulatory importance.
Leg. The metatarsal skin is characterized by
the presenceof a dense network of veins located
directly beneath the epidermis (Fig. 30. The veins
are a little smaller and appear more irregular in
outline than those in the naked skin of the head.
As in the head, the superficial venous plexus in
the feet doesnot appear to be supplied by typical
AVAs. AVAs were, however, encounteredamong
the larger, more deeply located blood vessels.
TEMPERATURE MEASUREMENTS
Head and neck. As Table 1 shows, crown and
nape skin temperatures were close to T, and to
T,, respectively. Both were higher at 40°C T, and
lower at 10°C T, than they were at 30°C T,.
Wing. The temperature profiles recorded in
one vulture are shown in Figure 6. Over the locm length of the humeral plexus, temperature
decreased,from T, at the proximal end, to 38,
34, or 22°C at the distal end, at T, of 40, 30, or
10°C respectively. At 10°C T,, the temperature
decrease along the plexus was nonlinear,
amounting to about 5°C in the first 6 cm, and
TURKEY VULTURE VASCULATURE
AND THERMOREGULATION
509
FIGURE 3. Histological sectionsof different skin areas and arteriovenous heat-exchangesystemsin Turkey
Vultures. a, the ophthalmic rete. b, crosssectionof the arteriovenousheat-exchangesystemin the wing. c, section
of the arteriovenousheat exchangerin the leg. d, skin on the feathered part of the neck. e, crown skin with a
superficialvenous plexus. f, section of the metatarsal skin. Abbreviations: A, artery; E, epidermis; N, nerve; V,
vein. (Scalebars equal 0.5 mm in a-c and 0.1 mm in d-f.)
510
Z. ARAD, U. MIDTGARD
AND
M. H. BERNSTEIN
FIGURE 4. Diagram presenting ventral view of part of the right wing of a Turkey Vulture, showing the
structureand location of the hypothesizedarteriovenousheat-exchangesystem. Veins (black) have been drawn
only in part. Drawings from sectionshave been added to illustrate arteriovenousproximity in the proximal (bb) and distal parts(a-a) ofthe wing. 1, A. & V. ulnaris;2, A. & V. radialis; 3, V. basilica;4, A. radialis superficialis;
5, A. radialis profunda; 6, A. & V. ulnaris superficialis;7, V. ulnaris profunda. H, humerus; R, radius; U, ulna.
Scalebar equals 1 cm.
12°C in the last 4 cm. These changescorrespond
to thermal gradientsofabout 0.8”C/cm and 3.0°C/
cm, respectively. The gradients at 30°C and 40°C
were linear and amounted respectivelyto 0.46”C/
cm and 0.25”C/cm. In the second vulture, the
gradients were smaller, but changed with T, in
the same manner.
BEHAVIORAL OBSERVATIONS
At T, of 10°C an unrestrained Turkey Vulture
kept the undersides of its wings in close contact
with its body, its head tilted downward, its neck
retracted, and the skin of its crown wrinkled, the
skin of its head and feet had a pale red color. At
20°C T,, no visible changes occurred. At 30°C
T,, the head was horizontal, the crown was less
wrinkled, the neck feathers were erect, and the
head and feet skin were redder. At 40°C T,, the
wings were extended with their undersides not
in contact with the body, the head was extended
with the neck exposed, and their color was deep
red. At 45°C T,, the vulture adopted a drooped-
wing posture, panted (160 mini) with its mouth
open, and urinated on its legs. At 50°C T,, synchronous panting and shallow gular fluttering
were observed. At this stage, water was offered
and the bird drank freely. At 53°C T,, the wings
were held farther from the body. After 90 min
at this T,, T, was 4 1.7%. When T, was returned
to 35°C T, decreased to 39.5”C but posture
changed little.
DISCUSSION
This study provides a detailed description of the
major blood vessels,AV heat-exchangesystems,
TURKEY VULTURE VASCULATURE
511
AND THERMOREGULATION
TABLE 1. Core body temperature (TJ, and subcutaneous temperatures at the crown (T,,,,.) and nape
(T,,,) at different ambient temperatures(TJ in a Turkey Vulture. Values are the means of steady-statetemperatures(range ? 0.2”C) recordedfor at least 16 min.
All temperaturesin “C.
10
30
40
39.5
38.7
40.3
13.8
31.6
39.8
36.8
37.5
39.5
HEAD AND NECK
The head is equipped with well-developed
ophthalmic retia, though the number of blood
vessels in each rete is lower than that reported
for other falconiform birds (Midtgsrd 1983). The
ophthalmic retia of birds have been shown to
cool the arterial blood to the brain (Kilgore et
al. 1979, Bernstein et al. 1979), thus reducing the
risk of heat stroke when T, is elevated during
heat exposure or exercise. It has also been suggestedthat the ophthalmic retia, like the AV heatexchangesystemsin the limbs, reduce heat loss
from the skin of the head in cold environments
(Frost et al. 1975). Although this would seem to
have particular value in a bird with an unfeathered head, it could function only for the periorbital skin, since the rete supplies blood only to
this region (Fig. 2).
The vascularization of the bare cephalic skin
in Turkey Vultures doesnot resemble that in the
red skin of gallinaceousbirds. Whereas the comb
and wattles of domestic fowl contain a multilayered capillary network (Lucas and Stettenheim
----_--___
._
_
bI
421
”
I
I
I
,
,
I
.
k!
FIGURE 5. Cranial view of the main veins (black)
and arteries in the right leg of a Turkey Vulture. The
sectionsa-a and b-b illustrate arteriovenousproximity.
1, A. & V. poplitea; 2, A. & V. tibialis caudalis;3, A.
tibialis cranialis; 4, A. & V. fibularis superficialis;5,
Rete tibiotarsale;6, A. & V. metatarseadorsalis;7, V.
metatarsea superficialis medialis. Scale bar equals 1
cm.
and skin vascularization in the head, neck, wing,
and leg of Turkey Vultures. The following discussion considers the findings as they relate to
local and general thermoregulation.
36---.-
l -N
-‘..-\----._-.
-.
5
E
,
,
I
To = 4OT
-.--___
To = 30-c
---*__
.*.
34
-.
\
--1
1
DISTANCE FROM SHOULDER JOINT, cm
FIGURE 6. Temperaturesrecordedat intervals along
the humeral vascularplexus, measuredas the distance
from the shoulderjoint, in a Turkey Vulture exposed
to ambient temperatures(TJ of 40, 30, or 10°C.
512
Z. ARAD,
U. MIDTGhD
AND
M. H. BERNSTEIN
1972) the naked skin of the vulture is characterized by large, superficial veins. The cephalic
venous plexus of the Turkey Vulture is also different from the collar plexus of pigeons which is
located subcutaneouslyand receivesblood from
AVAs (Baumel et al. 1983). The plexusesof both
the pigeon and the vulture apparently function
in thermoregulation.
It would be expected that vasodilation of the
venous plexus in the skin of the head would aid
heat lossduring high-temperature stress,and that
vasoconstriction would serve in heat conservation in the cold. These expectations are consistent with the behavioral observations: at high T,,
the head and neck were extended and the bare
skin changed color to deep red, during cold exposure, the crown and nape skin appeared wrinkled and pale. In addition the subcutaneoustemperature of the crown and nape increased
significantly and approachedcore T, during heat
stress,whereas during cold exposure crown and
nape skin temperatures decreased significantly,
the decrease in the former being more pronounced than in the latter (Table 1).
Brain temperature in Helmeted Guineafowl
(Numida meleagris)varied widely and was
strongly affected by the thermal environment
(Crowe and Withers 1979, Withers and Crowe
1980). These birds could regulate heat loss and
heat gain through the naked head skin by extending and retracting their heads, and in this
respect were similar to the Turkey Vultures in
the present study and to Black Vultures studied
previously by Larochelle et al. (1982). The cephalic skin thus seemsto play an important role
in temperature regulation by birds with unfeathered heads.
WING
The vascular anatomy of the wing has been studied in only a few species,and information about
AV associationsis limited to some penguins. In
the proximal part of penguin forelimbs a rete
mirabile with presumed heat-conserving function has been documented. Its arteries number
from three to five in smaller speciesand about
15 in Emperor Penguins, Aptenodytes
forsteri
(Watson 1883, Trawa 1970, Frost et al. 1975).
This structure has been implicated in heat conservation by penguins diving in cold water.
The present study demonstrates for the first
time a similar heat exchanger in the wings of a
strictly terrestrial, flying bird. In contrast with
penguins, the heat exchangerin vulture wings is
a well-developed venae comitantes system,completely enveloping the ulnar and radial arteries
and equipped with a large shunt vein, the vena
basilica. This venae comitantes system closely
resembles that in the feet of ravens (Midtgard
198 1) and in the fins of whales (Scholander and
Schevill 1955).
Our temperature measurements along the humeral vascular complex (Fig. 6) strongly suggest
that this structure functions as a heat exchanger.
The temperature gradient increased from about
O.S”C/cm at thermoneutrality to about 3“Ucm
in the distal segment during cold exposure. On
heat exposure, the gradient decreasedsuch that
the temperatureat the distal end waswithin about
2°C of T,. We hypothesizethat venous blood flow
is directed through the plexus during cold exposurebut bypassesit during heat exposure.The
vulture results resemble those obtained in the
forelimb of slothsby Scholanderand Krog (1957),
but the maximum gradient in the vulture was
greater than in the sloth. The heat-exchange efficiency of the vulture’s venae comitantes system
is thus at least equal to that of the sloth’s rete,
but this needs confirmation by additional measurement of temperature and blood flow.
It has been suggestedthat the ventral side of
the wing constitutesan important avenue for heat
dissipation (Eliassen 1963); this is consistentwith
the spread-wingpostureobservedin heat-stressed
Turkey Vultures. Our histological examination
of underwing skin, however, did not show anything similar to the conspicuousvascularization
of the head and leg. It is possible, especially during flight, that convection cools the large, superficially located veins, enhancing body cooling,
and this would be enhanced by soaring in cooler
air at high altitudes (Madsen 1930). It is also
possible that evaporative or convective cooling
of the dorsolateral thoracic surfacesis enhanced
when they are exposedby wing spreading.
LEG
The AV heat-exchangesystemin the legsof Turkey Vultures is similar to that observedin cranes,
ibises, and owls, and has been called a simple
rete becauseof its small number of blood vessels
(Midtgard 198 1). As in other birds, the large tibial vein bypassesthe heat exchangerand may be
the preferred route for venous return when heat
dissipation is called for.
The feet of birds are excellent dissipators of
TURKEY VULTURE VASCULATURE
excessbody heat (Steen and Steen 1965, Bemstein 1974, Kilgore and Schmidt-Nielsen 1975,
Baudinette et al. 1976, Midtgard 1980) and are
characterized by extensive skin vascularization
and many AVAs (Midtgard 1986). In the present
study, AVAs were found deep in the metatarsal
skin, so they are apparently not involved in the
filling of the superficial venous plexus. Nevertheless, this plexus undoubtedly has a thermoregulatory function, as suggestedby the color
changesof the metatarsal skin when T, was elevated and by the habit of urinating on the legs
during heat stress.
Kahl (1963) documented the latter phenomenon in heat-exposed Wood Storks (Mycteria
americana) and showedthat it plays a major role
in temperature regulation in this species.Hatch
(1970) verified Kahl’s (1963) suggestion that
urohidrosis also occurs in related New World
vultures and found that, as in the Wood Stork,
leg wetting contributes importantly to temperaature regulation in heat-exposed Turkey Vultures. Taken together, leg vascular anatomy and
urohidrosisin unrestrainedTurkey Vultures point
to an important role for the legs in this species’
temperature regulation.
CONCLUSIONS
We have demonstrated extensive skin vascularization in the unfeathered head, neck, and feet;
and well-developed AV heat exchangersin the
head, wings, and legs of Turkey Vultures. We
have provided preliminary support for the presumed thermoregulatory role of some of these
structuresby temperature measurementsand behavioral observations. The unrestrained, freely
moving bird regulated T, over a wide range of
T, ( 1O-5 3°C) by both physiological and postural
adjustments. In contrast, Turkey Vultures confined in a metabolic chamber relied exclusively
on physiological adjustments to maintain T,
(Arad and Bernstein 1988). Results of experiments under suchconditions therefore represent
only a part of the thermoregulatory adaptations
of this species.The full range of adaptations explains the ability of Turkey Vultures to live in
climates characterizedby a wide range of thermal
conditions.
ACKNOWLEDGMENTS
We thank B. Pinshow for his technical help, useful
advice, and stimulatingdiscussion.This studywassupported in part by a Danish-Israeli Scientific Exchange
AND THERMOREGULATION
513
Fellowship (ZA), a grant from the CarlsbergFoundation (UM), and by grant DCB-8402659 from the U.S.
National ScienceFoundation (MHB).
LITERATURE
CITED
ARAD,Z., AND M. H. BERNSTEIN.1988. Temperature
regulation in Turkey Vultures. Condor 90:913919.
BAUDINETTE,
R. V., J. P. LOVERIDGE,K. J. WILSON,
ANDK. SCHMIDT-NIELSEN.1976. Heat lossfrom
feet of Herring Gulls at rest and during flight. Am.
J. Physiol. 230:920-924.
BAUMEL,J. J., A. F. DALLEY,ANDT. H. QUINN. 1983.
The collar plexus of subcutaneousthermoregulatory veins in the pigeon, Columbalivia; its association with esophagealpulsationand gularflutter.
Zoomornholonv 102:215-239.
BAUMEL,J. J.: A. S%NG, A. M. LUCAS,J. E. BREAZILE,
AND H. E. EVANS. 1979. Nomina Anatomica
Avium. Academic Press,London.
BERNSTEIN,
M. H. 1974. Vascular responsesand foot
temperaturein pigeons.Am. J. Physiol. 226: 13501355.
BERNSTEIN,
M. H., I. SANDOVAL,M. B. CURTIS,AND
D. M. HUDSON. 1979. Brain temperature in pigeons: Effects of anterior respiratory bypass. J.
Comp. Physiol. 129:115-l 18.
CROWE,T. M., ANDP. C. WITHERS. 1979. Brain temperature regulation in Helmeted Guineafowl. S.
Afr. J. Sci. 75:362-365.
ELIASSEN,E. 1963. Preliminary results from new
methods of investigatingthe physiology of birds
during flight. Ibis 105:234~237._
_FROST.P.G.H., W. R. SIEGFRIED,AND P. J. GREENW&D. 1975. Arteriovenous.heat exchange sysdemersus.
tems in the JackassPenguin Spheniscus
J. Zool. 175:231-241.
HATCH,D. E. 1970. Energyconservingand heat dissipating mechanismsof the Turkey Vulture. Auk
87:111-124.
HEATH,J. E. 1962. Temperature fluctuation in the
Turkey Vulture. Condor 64~234-235.
KAHL.M. P.. JR. 1963. Thermoreaulationin the Wood
Storkw&hspecialreferenceto the role of the legs.
Physiol.Zool. 36:141-151.
K~LGORE,
D. L., JR.,D. F. BOGGS,
ANDG. F. BIRCHARD.
1979. Role of the retemirabileophthalmicum
in
maintaining the body to brain temperature difference in pigeons.J. Comp. Physiol. 129:119-122.
K~LGORE,
D. L., JR., ANDK. SCHMIDT-NIELSEN.1975.
Heat lossfrom ducks’feet immersed in cold water.
Condor 77~475478.
LAROCHELLE,
J., J. DELSON,AND K. SCHMIDT-NIELSEN.
1982. Temperature regulation in the Black Vulture. Can. J. Zool. 60:491494.
LUCAS,A. M., AND P. R. STETTENHEIM.1972. Avian
anatomy. Integument. Part II. Agriculture Handbook 362. U.S. Department of Agriculture, Washington, DC.
MADSEN,H. 1930. Quelquesremarquessur la cause
pourquoi les grands oiseaux au Sudan planent si
hautau milieu de lajournee.Vidensk. Medd. Dansk
Naturhist Foren. 88:301-303.
MIDTG~D, U. 1980. Heat lossfrom the feet of Mal-
514
Z. ARAD, U. MIDTGhD
AND
M. H. BERNSTEIN
lards Anasplatyrhynchosand arterio-venous heat
exchangein the retetibiotarsale.Ibis 122:354-359.
MIDTG.&D, U. 1981. The rete tibiotarsaleand arteriovenous associationin the hind limb of birds: a
comparative morphologicalstudyon counter-current heat exchangesystems.Acta Zool. (Stockh.)
6267-87.
MIDTG~D, U. 1983. Scalingof the brain and the eye
cooling systemin birds: A morphometric analysis
of the rete ophthalmicum.J. Exp. Zool. 225: 197207.
MIDTG.&RD,U. 1984. Blood vesselsand the occurrence of arteriovenous anastomosesin cephalic
heat loss areas of Mallards, Anas platyrhynchos
(Aves). Zoomorphology 104:323-335.
MIDTG~D, U. 1986. The peripheral circulatory system in birds. A morphological and physiological
study of some adaptationsto temperatureregulation. Ph.D.diss. Univ. of Copenhagen,Denmark.
MIDTG~D, U. 1988. Comparative morphology of
the avian circulatory system. Proc. XIX Int. Ornithol. Congr. (1986):2445-2454.
SCHOLANDER,
P. F., AND J. KRoG. 1957. Countercurrent heat exchange and vascular bundles in
sloths. J. Appl. Physiol. 10:405-411.
SCHOLANDER,
P. F., AND W. E. SCHEVILL. 1955.
Counter-currentvascularheat exchangein the fins
of whales. J. Appl. Physiol. 8~279-282.
STEEN,I., AND J. B. STEEN. 1965. The importance of
the legs in the thermoregulation of birds. Acta
Physiol. Stand. 63:285-29 1.
TRAWA,G. 1970. Note preliminaire sur la vascularisation desmembresdesspheniscidesde terre adelie. Oiseau Rev. Fr. Omithol. 40:142-156.
WATSON,M. 1883. Report on the anatomy of the
Spheniscidae.Report on the Scientific Research
of the Voyage of H.M.S. Challenger,Zoology 7: l242.
WITHERS,P. C., ANDT. M. CROWE. 1980. Brain temperaturefluctuationsin Helmeted Guineafowl under seminatural conditions. Condor 82:99-100.